Correspondence: Tawin Inpankaew, Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok 10900, Thailand.
Tel/Fax: 66 (0) 2942-8438
E-mail: [email protected], [email protected]
INTRODUCTION
It is common in Thailand to leave or aban- don unwanted dogs in temple grounds. Since temples are public places of worship and the donation of gifts, the owners trust that their animals will be fed and will be taken cared of by monks and nuns, as well as good-hearted temple visitors such as people who live nearby the temple grounds or people who love ani- mals and come to temple to feed them. Temple grounds in Thailand are generally sizeable with free access to the public and therefore seem to be a perfect place for unwanted animals.
At a minimum, the dogs can live on the left- over food of the monks. Under these circum-
CANINE PARASITIC ZOONOSES IN BANGKOK TEMPLES
Tawin Inpankaew1, Rebecca Traub2, RC Andrew Thompson3 and Yaowalark Sukthana4,5
1Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand; 2 School of Veterinary Science, University of Queensland, St Lucia, Queensland, Australia; 3WHO Collaborating Center for the Molecular Epidemiology of Parasitic Infections,
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Australia;
4Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; 5International College, Mahidol University, Bangkok, Thailand
Abstract. Fecal samples were collected from 204 humans and 229 dogs from 20 different temples in Bangkok, as well as communities in the surrounding temple ground areas. Human and dog stool samples were examined for intestinal parasites including Giardia using zinc sulfate flotation and microscopy. Hookworms were the most common parasite in dogs (58.1%) followed by Trichuris (20.5%), Isospora (10%), Giardia (7.9%), Toxocara (7.4%), Dipylidium caninum (4.4%) and Spirometra (3.1%). Blastocystis hominis (5.9%) was the most common parasite in humans followed by hookworms (3.4%), Giardia (2.5%), Strongyloides (2%) and Cryptosporidium (1.5%). All samples microscopy-positive for Giardia were genotyped. The majority of Giardia isolated from the dog population was placed in Assemblage A, followed by Assemblages D, B and C, respectively, while human isolates were placed in Assemblages A and B. Therefore, dogs in temple communities posed a potential zoonotic risk to humans for transmission of hookworms, Giardia (especially Assemblage A genotypes) and Toxocara canis.
stances, the population of semi-domesticated and stray dogs is high in temple communi- ties. This coupled with poor hygienic practices and overcrowded conditions, places the monks, nuns and people living in the surround- ing communities at a high risk of acquiring zoonotic parasites either directly through close contact with the dogs, or indirectly through the highly contaminated environment.
Surveillance data with regard to preva- lence of zoonotic canine gastrointestinal para- sites in Thailand is largely lacking. Previous s t u d i e s c o n d u c t e d b y H i n z ( 1 9 8 0 ) a n d Rojekittikhun et al (1998) found hookworms, Trichuris vulpis and Toxocara canis to be the most common parasites in stray dogs from Bangkok. Another study by Wiwanitkit and Waenlor (2004) found 5.7% of soil samples collected from Bangkok to be contaminated with Toxocara eggs. Semi-domesticated dogs in rural communities in Thailand have also
shown to act as potential reservoir hosts for the fish-borne parasites such as Gnathostoma spinigerum (Maleewong et al, 1992) and Opisthorchis viverrini. No data exist with re- gards to the prevalence of Giardia in dogs in Thailand.
Giardia duodenalis is a flagellated proto- zoan that inhabits the small intestine of hu- mans and other mammals. It is distributed worldwide and considered the most com- monly detected intestinal parasite in humans in developed countries (Schantz, 1991). In developing regions of the world, Giardia con- stitutes part of the complex group of parasitic, bacterial and viral diseases that impair the ability to achieve full potential and impair de- velopment and socio-economic improvement.
All diseases included in the WHO Neglected Diseases Initiative have a common link with poverty and as the current view is to take a comprehensive approach to all these dis- eases, Giardia was included (Savioli et al, 2006). Giardia is also considered a re-emerg- ing infectious agent because of its role in out- breaks of diarrhea in child-care centers (Thompson, 2000). Giardia is a zoonotic agent (Milstein and Goldsmid, 1997: Thompson et al, 2000); the organism is transmitted fecal- orally producing environmentally resistant cysts that are voided in the feces and may be transmitted directly via person-to-person or animal-to-person contact or indirectly via con- taminated food and water. There is in- creasing evidence in support of the zoonotic potential of canine Giardia with a growing number of studies identifying potentially zoonotic genotypes of Giardia in dogs and humans from both developed and disadvan- taged communities worldwide (Traub et al, 2004; Eligio-Garcia et al, 2005; Lalle et al, 2005). In Thailand, recent surveys addressed Giardia infection only in humans with a preva- lence of 5.3-14.36% (Nuchprayoon et al, 2002; Waikagul et al, 2002; Sirivichayakul et al, 2003). The prevalence of Giardia in animals,
however, is unknown. Information regarding the epidemiological status of zoonotic canine Giardia infection in dogs and humans in Thai- land is needed. In this study, we aim to deter- mine the prevalence of canine gastrointesti- nal parasites in canine and human populations in temples and their surrounding communities in Bangkok, with particular emphasis on the zoonotic potential of Giardia.
MATERIALS AND METHODS
Collection of fecal samples
Single fecal samples were collected from 204 humans and 229 dogs from 20 temples and their surrounding communities in the city of Bangkok. After informed consent, the ques- tionnaires were administered to the appropri- ate personnel with regard to risk factors for parasitic infection, including socio-economic status, crowding, age, gender, defecation practices, dog ownership and current signs of diarrhea. Fecal samples were preserved separately in 5% formalin for microscopic screening and 20% dimethyl sulfoxide for molecular testing.
Parasitological techniques
Human and dog fecal samples were ex- amined for the presence of parasites and Gia- rdia cyst using zinc sulfate and sodium nitrate flotation and microscopy (Faust et al, 1938).
Giardia cyst were then concentrated and pu- rified from microscopically positive human and dog samples using a saturated salt and glu- cose method (Meloni and Thompson, 1987).
Molecular methods
DNA extraction. The purified Giardia cysts were transferred into a 1.5 ml Eppendorff tube and centrifuged at 20,000g. Extraction of the Gia- rdia cysts was then carried out using QiAMP DNA Mini Stool Kit (Qiagen GMBH, Hilden, Germany).
The SSU-rDNA gene. A nested PCR was used to amplify a 300 bp region of SSU-rDNA gene
using primer AL4303, AL4305 and AL4304 and AL4306. Amplification conditions were carried out as previously described by Sulaiman et al (2003) and was used to geno- type all microscopic positive samples in this study.
Sequencing of PCR product. All PCR-positive samples were subjected to sequencing. PCR products were purified using Qiagen spin col- umns (Qiagen, Hilden, Germany) and se- quenced using an ABI Terminator Cycle Se- quencing Kit (Applied Biosystems, CA, USA) according to manufacturer’s instructions (GeneWorks, Australia). Sequences were analysed using SeqEd (Applied Biosystems, CA, USA) and aligned with each other as well as previously published sequences for G.
duodenalis isolates using Clustal W (Thomp- son et al, 1994).
Molecular characterization and phylogenic analysis. Distance-based analyses were per- formed using MEGA version 2.1 (Kumar et al, 2001). Distance-based analysed were con- ducted using Tamura-Nei distance estimates and trees were constructed using the Neigh- bor-Joining algorithm.
Statistical analysis
Univariate associations between the prevalence of Giardia in humans and dogs utilizing microscopic examination and PCR and host, behavioral and environmental fac- tors were initially made using chi-square re- sults for independence and ANOVA (continu- ous variables). Logistic multiple regression was used to quantify the association between the prevalence of Giardia using each test and each variable after adjusting for other variables.
Pearson’s correlation was utilized to determine the subfactors or variables that were highly associated with whether individual humans and animals belonged to the monastery or in- dividual households and these variables were tested for significance. Only variables signifi- cant at p ≤ 0.25 in the univariate analyses were
considered eligible for inclusion in the logistic multiple regression (Hosmer and Lemeshow, 1989; Frankena and Graat, 1997). Backward elimination was used to determine which fac- tors could be dropped from the multivariable model. The likelihood- ratio chi-squared sta- tistic was calculated to determine the signifi- cance at each step of the model building. The level of significance for a factor to remain in the final model was set at 10%. The good- ness of fit of the model was assessed with the Hosmer-Lemeshow statistic (Lemeshow and Hosmer, 1982). Data were analysed and statistical comparisons were performed using SPSS (SPSS for Windows, Version 14.0, Rain- bow Technologies) and Excel 2002 (Microsoft).
RESULTS
Survey results and intestinal parasites preva- lence
Eighty percent of dogs belonged to monks in the temple, and 20% of dogs be- longed to households surrounding the temple.
Ten and a half percent of dogs were puppies
< 4 months, 23.5% young adult dogs between 5-12 months of age, 56% adult dogs between 1-7 years of age and 10% geriatric dogs > 7 years old. Thirty-three percent of dogs were entire males, 6% sterilized males, 35.5% en- tire females, 14.0% sterilized females, 2% lac- tating females and 9.5% females of unknown sterilization or pregnancy status. Ninety-three percent of dogs were of mixed breed and the rest pure bred dogs. The majority of dogs (79.5%) had been vaccinated against rabies.
Fifty-eight percent of participants were monks or nuns belonging to the monastery, and the rest were families from households surrounding the Temple grounds. The mean age of individuals was 32.7 years with 18%
being < 10 years of age, 10% between 11-20 years of age, 22.5% between 21-30 years of age, 10.3% between 31-40 years of age, 17.7% between 41-50 years of age and 21.5%
above the age of 50 years. Sixty-six percent of participants were male and 34% female.
The majority of people defecated in indoor la- trines (95.6%), 3.4% defecated in indoor la- trines that directly emptied into the Chao Phraya River and 1% admitted to defecating outdoors. Commercial bottled water was drunk by 58% of participants, 28% drunk boiled or filtered tap water and 14% drunk untreated tap water.
Hookworms (58.1%, 95% CI = 51.7-64.5) were the most common parasite of dogs fol- lowed by Trichuris (20.5%, 95% CI = 15.3- 25.8), Isospora spp (10%, 95% CI = 6.2-13.9), Giardia spp (7.9%, 95%CI = 4.4-11.3), Toxo- cara canis (7.4%, 95%CI = 4-10.8), Dipylidium caninum (4.4%, 95%CI = 1.7-7) and Spirometra (3.1%, 95%CI = 0.8-5.3). In humans, Blastocystis hominis was the most common parasite (5.9%, 95% CI = 2.7- 9.1), hook- worms–(3.4%, 95%CI = 0.9-5.9) followed by Giardia (2.5%, 95% CI = 0.9-5.9), Strongyloides (2%, 95% CI = 0.1-3.9) and Cryptosporidium (1.5%, 95%CI = 0-3.1). Most individuals def- ecated in proper indoor latrines (96%) and wore footwear while outdoors (92.5%).
Age was found to be the only significant risk factor for infection with Giardia and Toxo- cara in dogs. Dogs less than 4 months of age were more likely to be infected with Giardia than dogs that were older (OR= 4.6, 95% CI
= 1.5- 13.7, p = 0.01). Similarly, dogs less than one year were more likely to be infected with Toxocara canis than older dogs (OR= 5.2, 95% CI = 1.7-15.3, p = 0.01). Dogs less than one year (OR 2.1, 95% CI, 1.0-4.1, p = 0.04), those living in the immediate surroundings of more than 10 dogs (OR 2.8, 95% CI, 1.0-7.4, p = 0.04), those that were not dewormed at least once in the past 12 months (OR 7.2, 95%
CI, 2.7-19.2, p = 0.00), and those that were entire animal (OR 3.1, 95% CI, 1.5-6.7, p = 0.00) were more likely to be infected with hookworms. Finally, dewormed dogs (OR 3.9, 95% CI 0.9-17.5, p = 0.07) and those living in
the immediate surroundings of less than 10 dogs (OR 4.8, 95% CI 1.1-20.0, p = 0.04) were also more likely to harbor Trichuris vulpis.
In humans, risk factors of significance were only found for infection with Giardia. All Giardia positive individuals were children be- low 6 years old. Apart from one child suffer- ing from anorexia no other child complained of any associated clinical symptoms of giar- diasis. Only univariate analysis was conducted for humans positive for Giardia by ZME as there were too few samples positive for Giar- dia to enable multivariate analysis. The mean age of Giardia positive individuals was 4.36 years compared to 33.4 years for Giardia negative individuals (p = 0.002). Individuals drinking untreated tap water were 2.46 times (95% CI = 0.8-2.91) more likely to be positive for Giardia using ZME than those drinking ei- ther treated tap water or commercially bottled water (p = 0.012).
Molecular characterization and phylogenetic analysis of Giardia isolates found in humans and dogs
In total, 3/5 and 13/18 microscopy posi- tive Giardia samples from humans and dogs respectively, were successfully amplified by PCR and sequenced at the SSU-rDNA gene.
Phylogenetic analysis of the 290 bp region of the SSU-rDNA data placed all of the dog iso- lates into the Assemblages A, B, C and D clus- ters and human isolates into Assemblages A and B clusters but was poor at resolving the relationships (Fig 1) between Assemblages B, C and D. The majority of Giardia isolates re- covered from the dog population were Assem- blage A followed by Assemblages D, then B and C, respectively. Three dogs had mixed in- fection with Assemblages A and BIII. Similar genotypes of G. duodenalis (Assemblage A) were recovered from a temple dog (T8D10) and monks (T8P7, T8P) within the same monas- tery. The majority of human Giardia isolates clustered into Assemblage A, while only one human (T8P8) had mixed infection with Assem-
Fig 1–Phylogeny of the Giardia isolates inferred by distance based analysis using Tamura-Nei distance esti- mates of alined nucleotide sequences derived from the PCR products of the SSU-rDNA gene (T= temple number, H= house number, D= dog number, P= human number) and boxes with bold outlines are humans isolates, those with normal outlines are dog isolates.
290 bp of 18-S loci
blages A and BIII.
DISCUSSION
The results of this study strongly support previous conclusions of Hinz (1980) and Rojekittikhun et al (1998), showing that dogs in temple communities of Bangkok pose an important zoonotic risk with regards to the transmission of hookworms and Toxocara canis. Humans become infected with Toxo- cara when they accidently ingest embryonated
eggs, usually through contaminated soil. Al- though most people infected with T. canis do not develop overt clinical disease, three clini- cal syndromes, namely visceral larva migrans, ocular larva migrans and covert toxocariasis in humans have been reported (reviewed by Irwin and Traub, 2006). Although the preva- lence of T. canis was lower than the other hel- minths (7.5%) the ability of these highly resis- tant eggs to withstand adverse conditions means that they may remain infective and ac- cumulate to high intensities in the environment
for a period of years. Similarly, larval stages of hookworms in soil may infect humans with exposed unprotected skin, manifesting prima- rily as cutaneous larva migrans or “creeping eruptions”. The majority of individuals in this community admitted to using footwear while outdoors. This method of control will need to be re-enforced within the community, espe- cially among children, given the high preva- lence of hookworms in dogs in this commu- nity coupled with poor environmental stan- dards of hygiene and widespread environmen- tal contamination.
This is the first study to reveal the preva- lence, transmission cycles and zoonotic poten- tial of Giardia in humans and dogs in Thailand.
However, it has been suggested that the preva- lence of Giardia using conventional methods such as zinc flotation and microscopy is often underestimated because of the low sensitivity of this diagnostic method. This may be exac- erbated due to the intermittent nature of cyst excretion and poor technical training of labo- ratory personnel (Dryden et al, 2006). There- fore microscopy negative samples should, in the future, also be screened using molecular as well as immunodiagnostic tests such as im- munofluorescence antibody testing (IFAT) against the cyst wall proteins and the coproantigen capture enzyme-linked immuno- sorbent assay (CELISA). Moreover, the diag- nostic methods utilized depend highly on the purpose of the study. If the aim of study is to determine the morbidity of giardiasis in clini- cally affected individuals (eg, children, elderly, immunologically naive) then the intensity of Gia- rdia cysts may be a better indicator and micro- scopic screening would be a more appropriate diagnostic tool.
The genetic characterization of Giardia isolates recovered from dogs and humans pro- vides supporting evidence for the occurrence of both zoonotic and non-zoonotic transmis- sion in this localized endemic focus. Analysis of the SSU-rDNA sequence data shows dog
populations to have two cycles of Giardia transmission; the first with a zoonotic cycle in which Giardia isolates belonging to Assem- blages A and B have a cycle among dogs and presumably humans, similar to a previous study in the tea growing communities in In- dia, where it was found that Assemblages A and B predominated in dogs (Traub et al, 2004). The second with a dog specific cycle in which dogs isolates of Giardia placed within Assemblages C and D have a cycle among dogs, similar to a previous study in aboriginal communities in Australia (Hopkins et al, 1997).
In temple communities in Bangkok, both zoonotic and non-zoonotic cycles of Giardia were circulating among dogs. The majority of dogs within the temple roam within packs with a high level of dog to dog contact. Dogs in this group were therefore likely to be shed- ding and transmitting Giardia Assemblages C and D from dog to dog. At the same time, these dogs and more so dogs from surround- ing households also had close contact with human populations and may be cycling Giar- dia isolates from Assemblages A and B both to and from humans and among each other.
The majority of dog isolates of G. duodenalis in dogs clustered into Assemblage A followed by Assemblages D, B and C, while human iso- lates were placed into Assemblages A or B.
Consequently dogs in temple communities pose a moderate zoonotic risk to humans with regards to transmission of Giardia, especially with Assemblage A. Traub et al (2004), Eligio- Garcia et al (2005), Itagaki et al (2005) and Lalle et al (2005) also found Giardia isolates from dogs within Assemblage A to be the most common and significant in terms of zoonotic risk. However, the question as to whether hu- mans or dogs are the primary source of G.
duodenalis Assemblages A and B isolates still remain unanswered. Even so, dogs act as reservoirs for human infection.
The majority of Giardia positive individu- als in this study, regardless of the method of
detection, were clinically asymptomatic. Pre- vious studies have shown that most humans positive for Giardia were suffering from chronic malabsorption (Jahidi, 1978). Malabsorption syndrome is especially significant in children with low nutritional status. In another study, Giardia infection in children was demonstrated to not necessarily be accompanied by diar- rhea (Read et al, 2002). In the present study the majority of participants were adult males, therefore they may already have immunity against Giardia, which explains why they did not show any clinical symptoms. However, when looking at the microscopy results, all Giardia positive individuals were children be- low the age of 6 years old, emphasizing the high intensity of this parasite in children which could be detected by microscopy. All of the participants in this study were clinically asymp- tomatic, so antiparasitic treatment is not nec- essarily advocated, however, advice for pre- venting further transmission is recommended.
In this study, multivariate risk factor analy- sis revealed that younger dogs were consis- tently more likely to be positive for parasites such as hookworms, Toxocara and Giardia.
Age related immunity could account for this finding; however, it must be noted that micros- copy alone was utilized to establish preva- lence. It is likely that the lower sensitivity of conventional flotation and microscopy com- pared to immunodiagnostic and molecular methods (McGlade et al, 2003; Cirak and Bauer, 2004) is only detecting high intensities of infection which again, is likely to be encoun- tered in younger animals, therefore putting bias on these risk factors for prevalence. Never- theless, the high intensities of parasite stages shed by younger animals and those animals in overcrowded environments, as well as ani- mals that were not de-wormed, make them a significant source of infection both directly and through environmental contamination. A ma- jority of these dogs in temple communities in Bangkok are vaccinated against rabies by
government veterinary assistants. Volunteer veterinarians also offer their services in some temple communities by mass treating the temple dogs with ivermectin injections every 6 months and de-sexing the male dogs. In- creased commitment from the government to ensure that this service is offered free across all 500 odd temples in Bangkok will signifi- cantly aid the control of canine parasitic zoonoses in these communities.
ACKNOWLEDGEMENTS
Authors would like to thank Miss Chantira Sutthikornchai, Dr Ryan O’Handley, Dr Carlyse Palmer, Associate Professor Ian Robertson and Dr Hannes Wickert for their help, sugges- tion and support. We also would like to thank all the dog owners, monks, nuns and people who cooperated in this study. This project was financially supported by the Australian Re- s e a rc h C o u n c i l , B a y e r A n i m a l H e a l t h , Leverkusen, Germany and Faculty of Tropical Medicine Research fund, Mahidol University.
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